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The Journal of Neurophysiology Vol. 86 No. 6 December 2001, pp. 2998-3010
Copyright ©2001 by the American Physiological Society
1Department of Neurobiology and Physiology, Institute for Neuroscience and 2Department of Engineering Sciences and Applied Mathematics, Northwestern University, Evanston, Illinois 60208
Golding, Nace L.,
William L. Kath, and
Nelson Spruston.
Dichotomy of Action-Potential Backpropagation in CA1 Pyramidal
Neuron Dendrites. J. Neurophysiol. 86: 2998-3010, 2001. In hippocampal CA1 pyramidal neurons, action
potentials are typically initiated in the axon and backpropagate into
the dendrites, shaping the integration of synaptic activity and
influencing the induction of synaptic plasticity. Despite previous
reports describing action-potential propagation in the proximal apical
dendrites, the extent to which action potentials invade the distal
dendrites of CA1 pyramidal neurons remains controversial. Using paired
somatic and dendritic whole cell recordings, we find that in the
dendrites proximal to 280 µm from the soma, single backpropagating
action potentials exhibit <50% attenuation from their amplitude in
the soma. However, in dendritic recordings distal to 300 µm from the soma, action potentials in most cells backpropagated either strongly (26-42% attenuation; n = 9/20) or weakly (71-87%
attenuation; n = 10/20) with only one cell exhibiting
an intermediate value (45% attenuation). In experiments combining dual
somatic and dendritic whole cell recordings with calcium imaging, the
amount of calcium influx triggered by backpropagating action potentials
was correlated with the extent of action-potential invasion of the
distal dendrites. Quantitative morphometric analyses revealed that the
dichotomy in action-potential backpropagation occurred in the presence
of only subtle differences in either the diameter of the primary apical
dendrite or branching pattern. In addition, action-potential backpropagation was not dependent on a number of electrophysiological parameters (input resistance, resting potential, voltage sensitivity of
dendritic spike amplitude). There was, however, a striking correlation
of the shape of the action potential at the soma with its amplitude in
the dendrite; larger, faster-rising, and narrower somatic action
potentials exhibited more attenuation in the distal dendrites (300-410
µm from the soma). Simple compartmental models of CA1 pyramidal
neurons revealed that a dichotomy in action-potential backpropagation
could be generated in response to subtle manipulations of the
distribution of either sodium or potassium channels in the dendrites.
Backpropagation efficacy could also be influenced by local alterations
in dendritic side branches, but these effects were highly sensitive to
model parameters. Based on these findings, we hypothesize that the
observed dichotomy in dendritic action-potential amplitude is conferred
primarily by differences in the distribution, density, or modulatory
state of voltage-gated channels along the somatodendritic axis.
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